Colonization-induced host-gut microbial metabolic interaction
Open accessAbstract
UNLABELLED: The gut microbiota enhances the host's metabolic capacity for processing nutrients and drugs and modulate the activities of multiple pathways in a variety of organ systems. We have probed the systemic metabolic adaptation to gut colonization for 20 days following exposure of axenic mice (n = 35) to a typical environmental microbial background using high-resolution (1)H nuclear magnetic resonance (NMR) spectroscopy to analyze urine, plasma, liver, kidney, and colon (5 time points) metabolic profiles. Acquisition of the gut microbiota was associated with rapid increase in body weight (4%) over the first 5 days of colonization with parallel changes in multiple pathways in all compartments analyzed. The colonization process stimulated glycogenesis in the liver prior to triggering increases in hepatic triglyceride synthesis. These changes were associated with modifications of hepatic Cyp8b1 expression and the subsequent alteration of bile acid metabolites, including taurocholate and tauromuricholate, which are essential regulators of lipid absorption. Expression and activity of major drug-metabolizing enzymes (Cyp3a11 and Cyp2c29) were also significantly stimulated. Remarkably, statistical modeling of the interactions between hepatic metabolic profiles and microbial composition analyzed by 16S rRNA gene pyrosequencing revealed strong associations of the Coriobacteriaceae family with both the hepatic triglyceride, glucose, and glycogen levels and the metabolism of xenobiotics. These data demonstrate the importance of microbial activity in metabolic phenotype development, indicating that microbiota manipulation is a useful tool for beneficially modulating xenobiotic metabolism and pharmacokinetics in personalized health care. IMPORTANCE: Gut bacteria have been associated with various essential biological functions in humans such as energy harvest and regulation of blood pressure. Furthermore, gut microbial colonization occurs after birth in parallel with other critical processes such as immune and cognitive development. Thus, it is essential to understand the bidirectional interaction between the host metabolism and its symbionts. Here, we describe the first evidence of an in vivo association between a family of bacteria and hepatic lipid metabolism. These results provide new insights into the fundamental mechanisms that regulate host-gut microbiota interactions and are thus of wide interest to microbiological, nutrition, metabolic, systems biology, and pharmaceutical research communities. This work will also contribute to developing novel strategies in the alteration of host-gut microbiota relationships which can in turn beneficially modulate the host metabolism.
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Numerous new studies have demonstrated dramatic effects driven by widely used medications such as metformin and statins on the bile acid pool, as well as on microbial signatures associated with disease.
“In addition to the focus on diet and the microbiota, numerous new studies have already demonstrated dramatic effects driven by widely used medications such as metformin and statins on the bile acid pool, as well as on microbial signatures associated with disease105,106.”
From Dietary metabolism, the gut microbiome, and heart failure (2019) · cites this paper as [105]
Coriobacteriaceae and Erysipelotrichaceae have previously been linked to obesity and lipid, primarily cholesterol, metabolism.
“Coriobacteriaceae and Erysipelotrichaceae – previously linked to obesity and lipid, primarily cholesterol, metabolism [43], [44], [45]”
From Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals (2016) · cites this paper as [45]
Increased levels of Coriobacteriaceae and Erysipelotrichaceae have been associated previously with changes in hepatic and lipid metabolism in humans and various rodent species.
“These increased levels have been associated previously with changes in hepatic and lipid metabolism in humans and various rodent species [44], [45], [53], [54], [55].”
From Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals (2016) · cites this paper as [45]
The observed changes to Coriobacteriaceae and Erysipelotrichaceae did not acutely impact lipid metabolism.
“suggesting that the observed changes to Coriobacteriaceae and Erysipelotrichaceae – previously linked to obesity and lipid, primarily cholesterol, metabolism [43], [44], [45] – did not acutely impact lipid metabolism.”
From Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals (2016) · cites this paper as [45]
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- Authors
- Claus, S. P., Ellero, S. L., Berger, B., Krause, L., Bruttin, A., Molina, J., Paris, A., Want, E. J., de Waziers, I., Cloarec, O., Richards, S. E., Wang, Y., Dumas, M.-E., Ross, A., Rezzi, S., Kochhar, S., Van Bladeren, P., Lindon, J. C., Holmes, E., & Nicholson, J. K.
- Affiliations
- Imperial College London (GB)
- INSERM, Unité Mixte de Recherche 775, Université Paris Descartes, IFR des Saints Pères, Paris, France
- Nestlé (Switzerland) (CH)
- Institut National de la Recherche Agronomique (FR)
- Nestlé Research Centre, NESTEC Limited, Vers-Chez-les-Blancs, Lausanne, Switzerland
- Corresponding author
- Claus, Sandrine P.
- Krause, Lutz
- Wang, Yulan
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2011-04-29
- Volume
- 2
- Issue
- 2
- Pages
- e00271-10
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC3045766
- OpenAlex
- W2089691332
- Cited by
- 414
- References
- 35
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 17 · 2023: 23 · 2022: 26 · 2021: 30 · 2020: 35 · 2019: 31 · 2018: 30 · 2017: 29 · 2016: 31 · 2015: 30 · 2014: 34 · 2013: 33 · 2012: 26
- FWCI
- 14.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Imperial College London
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacogenetics and Drug Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- gut microbiota, host-microbe metabolic interactions, microbial colonization, germ-free mice, hepatic lipid metabolism, glycogen synthesis, hepatic triglyceride synthesis, bile acid metabolism, CYP8B1, CYP3A11, CYP2C29, xenobiotic metabolism, Coriobacteriaceae, drug-metabolizing enzymes, weight gain
- MeSH terms
- Animals, Bacteria, Body Weight, DNA, Bacterial, DNA, Ribosomal, Female, Germ-Free Life, Kidney, Liver, Magnetic Resonance Spectroscopy, Plasma, RNA, Ribosomal, 16S, Urine, Sequence Analysis, DNA, Gastrointestinal Tract, Biodiversity, Mice
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